PECAM-1 is involved in BCR/ABL signaling and may downregulate imatinib-induced apoptosis of Philadelphia chromosome-positive leukemia cells

International Journal of Oncology

Volumn 42, Issue 2, 2013, Pages 419-428

  Wu, Nan ^a   Kurosu, Tetsuya ^a   Oshikawa, Gaku ^a   Nagao, Toshikage ^a   Miura, Osamu ^a  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

Author keywords

Apoptosis; BCR ABL; Imatinib; Leukemia; PECAM 1

Indexed keywords

BCR ABL PROTEIN; CASPASE 3; CD31 ANTIGEN; DASATINIB; IMATINIB; PROTEIN TYROSINE KINASE; SORAFENIB;

ACUTE LYMPHOBLASTIC LEUKEMIA; APOPTOSIS; ARTICLE; CELL ADHESION; CELL MEMBRANE DEPOLARIZATION; CELL VIABILITY; CHEMOSENSITIVITY; CHRONIC MYELOID LEUKEMIA; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; LEUKEMIA CELL; MITOCHONDRION; PHILADELPHIA CHROMOSOME POSITIVE CELL; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANTIGENS, CD31; APOPTOSIS; BENZAMIDES; CELL ADHESION; DRUG RESISTANCE, NEOPLASM; FUSION PROTEINS, BCR-ABL; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; K562 CELLS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; PHILADELPHIA CHROMOSOME; PIPERAZINES; PYRIMIDINES; SIGNAL TRANSDUCTION;

EID: 84873642281     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2012.1729     Document Type: Article

References (52)

1. Newman PJ: The biology of PECAM-1. J Clin Invest 99: 3-8, 1997.
2. Privratsky JR, Newman DK and Newman PJ: PECAM-1: conflicts of interest in inflammation. Life Sci 87: 69-82, 2010.
3. Ilan N and Madri JA: PECAM-1: old friend, new partners. Curr Opin Cell Biol 15: 515-524, 2003.
4. Jackson DE: The unfolding tale of PECAM-1. FEBS Lett 540: 7-14, 2003.
5. Dhanjal TS, Pendaries C, Ross EA, et al: A novel role for PECAM-1 in megakaryocytokinesis and recovery of platelet counts in thrombocytopenic mice. Blood 109: 4237-4244, 2007.
6. Ross EA, Freeman S, Zhao Y, et al: A novel role for PECAM-1 (CD31) in regulating haematopoietic progenitor cell compartmentalization between the peripheral blood and bone marrow. PLoS One 3: e2338, 2008.
7. Wheadon H, Edmead C and Welham MJ: Regulation of interleukin-3-induced substrate phosphorylation and cell survival by SHP-2 (Src-homology protein tyrosine phosphatase 2). Biochem J 376: 147-157, 2003.
8. Gallay N, Anani L, Lopez A, et al: The role of platelet/endothelial cell adhesion molecule 1 (CD31) and CD38 antigens in marrow microenvironmental retention of acute myelogenous leukemia cells. Cancer Res 67: 8624-8632, 2007.
9. Akers SM, O'Leary HA, Minnear FL, et al: VE-cadherin and PECAM-1 enhance ALL migration across brain microvascular endothelial cell monolayers. Exp Hematol 38: 733-743, 2010.
10. Ibrahim S, Jilani I, O'Brien S, et al: Clinical relevance of the expression of the CD31 ligand for CD38 in patients with B-cell chronic lymphocytic leukemia. Cancer 97: 1914-1919, 2003.
11. Tonino SH, Spijker R, Luijks DM, van Oers MH and Kater AP: No convincing evidence for a role of CD31-CD38 interactions in the pathogenesis of chronic lymphocytic leukemia. Blood 112: 840-843, 2008.
12. Goldman JM and Melo JV: Chronic myeloid leukemia - advances in biology and new approaches to treatment. N Engl J Med 349: 1451-1464, 2003.
13. Wong S and Witte ON: The BCR-ABL story: bench to bedside and back. Annu Rev Immunol 22: 247-306, 2004.
14. Gruber F, Mustjoki S and Porkka K: Impact of tyrosine kinase inhibitors on patient outcomes in Philadelphia chromosome-positive acute lymphoblastic leukaemia. Br J Haematol 145: 581-597, 2009.
15. Yamamoto M, Kurosu T, Kakihana K, Mizuchi D and Miura O: The two major imatinib resistance mutations E255K and T315I enhance the activity of BCR/ABL fusion kinase. Biochem Biophys Res Commun 319: 1272-1275, 2004.
16. Kurosu T, Tsuji K, Kida A, Koyama T, Yamamoto M and Miura O: Rottlerin synergistically enhances imatinib-induced apoptosis of BCR/ABL-expressing cells through its mitochondrial uncoupling effect independent of protein kinase C-delta. Oncogene 26: 2975-2987, 2007.
17. Kurosu T, Ohki M, Wu N, Kagechika H and Miura O: Sorafenib induces apoptosis specifically in cells expressing BCR/ABL by inhibiting its kinase activity to activate the intrinsic mitochondrial pathway. Cancer Res 69: 3927-3936, 2009.
18. Griswold IJ, MacPartlin M, Bumm T, et al: Kinase domain mutants of Bcr-Abl exhibit altered transformation potency, kinase activity, and substrate utilization, irrespective of sensitivity to imatinib. Mol Cell Biol 26: 6082-6093, 2006.
19. Skaggs BJ, Gorre ME, Ryvkin A, et al: Phosphorylation of the ATP-binding loop directs oncogenicity of drug-resistant BCR-ABL mutants. Proc Natl Acad Sci USA 103: 19466-19471, 2006.
20. Danhauser-Riedl S, Warmuth M, Druker BJ, Emmerich B and Hallek M: Activation of Src kinases p53/56lyn and p59hck by p210bcr/abl in myeloid cells. Cancer Res 56: 3589-3596, 1996.
21. Wu J, Meng F, Kong LY, et al: Association between imatinib-resistant BCR-ABL mutation-negative leukemia and persistent activation of LYN kinase. J Natl Cancer Inst 100: 926-939, 2008.
22. Quintas-Cardama A, Kantarjian H and Cortes J: Flying under the radar: the new wave of BCR-ABL inhibitors. Nat Rev Drug Discov 6: 834-848, 2007.
23. Klucher KM, Lopez DV and Daley GQ: Secondary mutation maintains the transformed state in BaF3 cells with inducible BCR/ABL expression. Blood 91: 3927-3934, 1998.
24. Tohda S, Sakashita C, Fukuda T, Murakami N and Nara N: Establishment of a double Philadelphia chromosome-positive acute lymphoblastic leukemia-derived cell line, TMD5: effects of cytokines and differentiation inducers on growth of the cells. Leuk Res 23: 255-261, 1999.
25. Morita S, Kojima T and Kitamura T: Plat-E: an efficient and stable system for transient packaging of retroviruses. Gene Ther 7: 1063-1066, 2000.
26. DuBridge RB, Tang P, Hsia HC, Leong PM, Miller JH and Calos MP: Analysis of mutation in human cells by using an Epstein-Barr virus shuttle system. Mol Cell Biol 7: 379-387, 1987.
27. Mizuchi D, Kurosu T, Kida A, et al: BCR/ABL activates Rap1 and B-Raf to stimulate the MEK/Erk signaling pathway in hematopoietic cells. Biochem Biophys Res Commun 326: 645-651, 2005.
28. Chin H, Arai A, Wakao H, Kamiyama R, Miyasaka N and Miura O: Lyn physically associates with the erythropoietin receptor and may play a role in activation of the Stat5 pathway. Blood 91: 3734-3745, 1998.
29. Kitamura T, Koshino Y, Shibata F, et al: Retrovirus-mediated gene transfer and expression cloning: powerful tools in functional genomics. Exp Hematol 31: 1007-1014, 2003.
30. Jackson DE, Kupcho KR and Newman PJ: Characterization of phosphotyrosine binding motifs in the cytoplasmic domain of platelet/endothelial cell adhesion molecule-1 (PECAM-1) that are required for the cellular association and activation of the protein-tyrosine phosphatase, SHP-2. J Biol Chem 272: 24868 24875, 1997.
31. Newman DK, Hamilton C and Newman PJ: Inhibition of antigen-receptor signaling by platelet endothelial cell adhesion molecule-1 (CD31) requires functional ITIMs, SHP-2, and p56(lck). Blood 97: 2351-2357, 2001.
32. Kolli S, Zito CI, Mossink MH, Wiemer EA and Bennett AM: The major vault protein is a novel substrate for the tyrosine phosphatase SHP-2 and scaffold protein in epidermal growth factor signaling. J Biol Chem 279: 29374-29385, 2004.
33. Oshikawa G, Nagao T, Wu N, Kurosu T and Miura O: c-Cbl and Cbl-b ligases mediate 17-allylaminodemethoxygeldanamycin-induced degradation of autophosphorylated Flt3 kinase with internal tandem duplication through the ubiquitin proteasome pathway. J Biol Chem 286: 30263-30273, 2011.
34. Miura O, Cleveland JL and Ihle JN: Inactivation of erythropoietin receptor function by point mutations in a region having homology with other cytokine receptors. Mol Cell Biol 13: 1788-1795, 1993.
35. Arai A, Nosaka Y, Kanda E, Yamamoto K, Miyasaka N and Miura O: Rap1 is activated by erythropoietin or interleukin-3 and is involved in regulation of beta1 integrin-mediated hematopoietic cell adhesion. J Biol Chem 276: 10453-10462, 2001.
36. Jin A, Kurosu T, Tsuji K, et al: BCR/ABL and IL-3 activate Rap1 to stimulate the B-Raf/MEK/Erk and Akt signaling pathways and to regulate proliferation, apoptosis, and adhesion. Oncogene 25: 4332-4340, 2006.
37. Newman PJ and Newman DK: Signal transduction pathways mediated by PECAM-1: new roles for an old molecule in platelet and vascular cell biology. Arterioscler Thromb Vasc Biol 23: 953-964, 2003.
38. Flint AJ, Tiganis T, Barford D and Tonks NK: Development of 'substrate-trapping' mutants to identify physiological substrates of protein tyrosine phosphatases. Proc Natl Acad Sci USA 94: 1680-1685, 1997.
39. Albelda SM, Muller WA, Buck CA and Newman PJ: Molecular and cellular properties of PECAM-1 (endoCAM/CD31): a novel vascular cell-cell adhesion molecule. J Cell Biol 114: 1059-1068, 1991.
40. Bergom C, Goel R, Paddock C, et al: The cell-adhesion and signaling molecule PECAM-1 is a molecular mediator of resistance to genotoxic chemotherapy. Cancer Biol Ther 5: 1699 1707, 2006.
41. Bird IN, Taylor V, Newton JP, et al: Homophilic PECAM 1(CD31) interactions prevent endothelial cell apoptosis but do not support cell spreading or migration. J Cell Sci 112: 1989 1997, 1999.
42. Ferrero E, Belloni D, Contini P, et al: Transendothelial migration leads to protection from starvation-induced apoptosis in CD34+CD14+ circulating precursors: evidence for PECAM 1 involvement through Akt/PKB activation. Blood 101: 186-193, 2003.
43. Gao C, Sun W, Christofidou-Solomidou M, et al: PECAM-1 functions as a specific and potent inhibitor of mitochondrial-dependent apoptosis. Blood 102: 169-179, 2003.
44. Limaye V, Li X, Hahn C, et al: Sphingosine kinase-1 enhances endothelial cell survival through a PECAM-1-dependent activation of PI-3K/Akt and regulation of Bcl-2 family members. Blood 105: 3169-3177, 2005.
45. Chan G, Kalaitzidis D and Neel BG: The tyrosine phosphatase Shp2 (PTPN11) in cancer. Cancer Metastasis Rev 27: 179-192, 2008.
46. Scherr M, Chaturvedi A, Battmer K, et al: Enhanced sensitivity to inhibition of SHP2, STAT5, and Gab2 expression in chronic myeloid leukemia (CML). Blood 107: 3279-3287, 2006.
47. Chen J, Yu WM, Daino H, Broxmeyer HE, Druker BJ and Qu CK: SHP-2 phosphatase is required for hematopoietic cell transformation by Bcr-Abl. Blood 109: 778-785, 2007.
48. Biswas P, Canosa S, Schoenfeld D, et al: PECAM-1 affects GSK-3beta-mediated beta-catenin phosphorylation and degradation. Am J Pathol 169: 314-324, 2006.
49. Coluccia AM, Vacca A, Dunach M, et al: Bcr-Abl stabilizes beta-catenin in chronic myeloid leukemia through its tyrosine phosphorylation. EMBO J 26: 1456-1466, 2007.
50. Hu Y, Chen Y, Douglas L and Li S: beta-Catenin is essential for survival of leukemic stem cells insensitive to kinase inhibition in mice with BCR-ABL-induced chronic myeloid leukemia. Leukemia 23: 109-116, 2009.
51. Shang YC, Zhang C, Wang SH, et al: Activated beta-catenin induces myogenesis and inhibits adipogenesis in BM-derived mesenchymal stromal cells. Cytotherapy 9: 667-681, 2007.
52. Meads MB, Hazlehurst LA and Dalton WS: The bone marrow microenvironment as a tumor sanctuary and contributor to drug resistance. Clin Cancer Res 14: 2519-2526, 2008.